Abstract

The nutritional effects on maternal blood metabolites levels and outcome of
pregnancy in goats were investigated. The supplementary diet (106g/kg crude
protein) was given to S animals at a rate of 400g/animal/d. Two weeks prior to
and at parturition, S (Supplemented) does were heavier (P<0.05) and were in
better (P<0.001) body condition than C (Control) animals.

Eighty-nine percent of
S animals kidded including abortions, while the value was 79 for C animals,
however the difference was not significant (P>0.05). Prolificacy was higher for
S but was not significantly different (P>0.05; 1.93±0.17 versus 1.64±0.18kid/doe
for S and C respectively). Percentage reproductive wastage was lower (P<0.05) in
S than C group. Birth weights were similar between S and C animals (P>0.05;
2.70±0.11 and 2.60±0.13kg). A significant (P<0.05) difference was recorded on
the concentrations of cholesterol, haematocrit, triiodothyronine (T3)
and tetraiodothyronine (T4) (P<0.01) between the groups, S animals
having high values than C animals.

It is discussed that infectious agents were
not a prime cause of reproductive wastage. Kid viability at birth contributed to
reproductive wastage and difference in T3 and T4 may be
involved but not cortisol. Supplementary feeding of pregnant goats grazing
natural pasture during the dry season can offset the detrimental effects of
maternal nutritional stress and therefore reducing reproductive wastage.

Introduction

Tswana goat is
a meat-type indigenous breed and was reported by Senyatso and Masilo (1996) to
account for 80% of the national goats’ population. The need to improve
productivity of Tswana goat is emphasized by the fact that this animal holds
promise to increase smallholder incomes and household nutrition. Past government
policies to improve small ruminant productivity included Financial Assistant
Policy (FAP) to cover small ruminant projects. However, the anticipated
increased productivity was never realised, mainly due to low level of husbandry
and feeding management (Letsebe et al1999)

Past studies
(APRU 1987, Gray 1987, APRU 1989 and Madibela et al 2002) reported frequency of
twinning in Tswana goat of 50% and this has been associated with rapid increases
in goat numbers. In addition short gestation period means that meat production
can be realized in a relatively shorter period of time. However, nutrition plays
a major role in the attainment of genetic potential for reproduction and growth.
Reproductive wastage in terms of abortion, fetal loss and neonatal loss
undermine productivity of goats in Botswana. There are reports of abortion and
foetal loss in goats elsewhere (Hussain et al 1996a, Hussain et al 1996b,
Engeland et al 1997, Romero-M et al 1998, and Engeland et al 1998). In Botswana,
abortion storms occur during the winter months, (Binta et al 1996) which
coincide with the dry season. Though infectious causes have been found in
aborting goats, these accounted for only 10% (Binta et al 1998a) and 23% (Binta
et al 1998b) of the total number of animals aborting. According to Binta et al
(1996), several infectious and non-infectious factors may be responsible for
causing abortions in goats in Botswana, but the majority of the abortion cases
have never been explained. Few cases of abortions are caused by infectious
agents in Norwegian dairy goats, (Hussain et al 1996a, Hussain et al 1996b) and
Engeland et al (1997) suggested that nutritional and environmental factors might
be important. Ahmadu (1996) reported incidents of abortion in Zaria area of
Northern Nigeria and attributed it to improper feeding of goats during
pregnancy. Underfeeding leads to nutritional stress and may affect hormonal
secretion associated with metabolisms. There is lack of information on the
effects of nutrition on the extent of reproductive wastage, cortisol and thyroid
hormones in Tswana goats in Botswana. Therefore present study investigated the
nutritional effects on maternal blood metabolites, cortisol and thyroid hormones
levels and on the outcome of pregnancy of dry season kidding Tswana goats.

Materials
and methods

Location of
study

The study was
conducted at Sebele Station which is situated at latitude of 24o 33'S
and longitude 25o 57' E, at an altitude of 994 m a.s.l. The
vegetation type of the area has previously been described by Madibela et al
(2000). Grass quality and quantity fluctuate with season, being adequate in
months of October-March (ONDJFM) and in short supply or low in quality in
April-September (AMJJAS), when browse supplies most nutrient requirements of
goats. Data for rainfall and temperature for Sebele were collected from Botswana
Meteorology Services weather station located approximately 0.5km from the study
site. Mean rainfall for the area is 500mm. Monthly average minimum and maximum
temperature is 12.8 and 28.6oC respectively.

Experimental animals and treatments

Thirty-seven Tswana goats (3-6
years of age) divided into two groups; (C; mean±SE 38.8±0.9kg, n=19) and (S;
39.8±0.9, n=18) were used in a trial that commenced in May 2000. The animals had
previously kidded in January and kids were weaned at the end of April. The
animals were cared for according to International Guidelines for Biomedical
Research Involving Animals (CIOMS 1985). They were treated for internal
parasites (Ivomec®, Logos Agvet; Republic of South Africa). A plunge dip was use
for tick control (9%v/v chlorfenvinphos concentrate, Agricura, Republic of South
Africa) only when infestation was observed. The supplementary diet has been used
previously for breeding goats (Madibela et al 2002) Chemical composition of the
supplementary feed and its estimated nutrient supply is shown on Table 1.

Table 1. Gross
energy, chemical composition and estimated nutrient intake/animal/d
from the supplemented feed at the start and two weeks prior to
parturition

Goats feed intake is about 4% of
their body weight (Kadzere et al 1996); so at the start of the trial it was
assumed that S animals were consuming 1.2kg from grazing while 0.4kg was
provided by the supplement. C animals were assumed to be getting the whole of
their 1.6 kg feed intake from grazing. The animals were accompanied by bucks
during grazing (one buck to 25 does), as is the case in the communal farming
system of Botswana. Due to the poor grazing conditions which lead to decline in
body condition of the animals two weeks prior to parturition, feed for the S
group (body condition score, BCS = 2.83 on a 1 to 5 scale, where 1=thin, 5=fat
as per Karua 1990) was increased from about 400 to 750g/animal/d while
the C group (condition score =1.89) were offered 600g/animal/d of feed to avoid
unnecessary suffering by the animals. Data records included monthly BCS, live
weights and birth weights. The numbers of does that delivered, fetal loss and
kid mortality were recorded.

Blood sampling and processing

Blood was
collected from five animals selected at random and sampled from each of the two
treatments during the last two weeks of pregnancy. Each doe was bled by jugular
vein puncture and blood collected in heparin coated and into plain vacutainers.
The blood was centrifuged at 3000 x g for 10 minutes and plasma was harvested,
stored at -20oC until analysed for triiodothyronine (T3),
tetraiodothyronine (T4) and cortisol. Serum was harvested from blood
samples from plain tubes by allowing them to stand for one hour at room
temperature. Serum was used in analysis for total protein, albumin, calcium,
phosphorous, copper, zinc, urea, cholesterol, triglycerides.

Analysis
for hormones

Thyroid
hormone concentrations were determined with commercial kits. T3 and T4
concentrations were measured in duplicate by solid phase 125I
radioimmunoassy according to the manufacturer’s instructions (Diagnostic
Products Corporation, Los Angeles, CA, USA). The radioactivity of
teraiodothyronine- and triiodothyronine-bound tubes was counted with a gamma
counter, as previously described (Chopra 1972). Cortisol was determined
using a solid phase technique GammaCoat 125I cortisol
radioimmunoassay kit (DiaSorin, Stillwater, Minnesita, USA). The procedure is
based on the competitive binding principles and a gamma counter was used to
estimate cortisol levels, as previously described (Rehbinder and Hau 2006).

Biochemical
analysis

Serum samples
were taken to the National Veterinary Laboratory (Gaborone, Botswana) where they
were analysed for copper, zinc (UV spectrophotometry), total protein, albumin,
calcium, phosphorous, urea, cholesterol and triglycerides (Automatic chemical
analyzer) according to methods described by Mushi et al(1998). Globulin
was calculated as a difference between total protein and albumin. Haematocrit
analysis was done using standard haematological procedures.

Statistical
analysis

General linear models (GLM) procedure (SAS Institute Inc. 1990) was used to
determine the effects of supplementation on body weight, condition score and
blood parameters. The effects of supplementation on pregnancy rate were
evaluated by frequency analysis, using a Chi-square test (SAS Institute Inc.
1990). The Fisher Exact Test was used when the number of animals in a treatment
category was less than five (Steel and Torrie 1980). Goats that did not give
birth were excluded from the analysis of body weight and BCS at two weeks prior
to parturition and at parturition and from analysis for reproductive wastage.
GLM procedure (SAS Institute Inc. 1990) was also used to test the effects of
supplementation on reproductive wastage including and then excluding animals
whose kids and/or fetuses died due to infectious cause. Effects of
supplementation on birth weight of kid, and correlations between doe parturition
weight and kid birth weight were tested. Because of low numbers of kids born as
singles this test was also repeated without singles. One animal from the Control
group died due to ingestion of plastic material and was found to be carrying
twin fetuses, but was excluded from reproductive wastage analysis. One animal
from the S group had an early abortion and only placental material was recovered
but no infectious microorganism was isolated. This animal too was excluded from
the analysis of body weight, BCS and reproductive wastage. Another animal from
the S group sustained a fracture just before it gave birth and thus was not
weighed at parturition. Reproductive wastage was defined as the number of
fetuses that were aborted, born dead or kids that died during the first 24
hours, per doe.

Results

The
percentages of animal in S and C treatment groups which either gave birth or
aborted were similar (P>0.05; Table 2).

Table 2. Effect of
supplementation on the outcome of mating and pregnancy of Tswana
goats

Parameter

Supplemented

Control

SL

No of goats at mating`

18

19

No of goats pregnant1

16

152

Pregnancy rate, %

88.9

78.9

NS

No of goats aborted

1

2

No goats with dead foetuses

0

2

No of goats whose kids dead
in first 24 hours

3

2

No of goats abortive
microorganism isolated

0

1†

Reproductive parameters

n=15

n=14

Prolificacy, kid/doe 3

1.93±0.17

1.64±0.18

NS

Total Wastage, kid/doe4

0.27±0.18

0.71±0.19

NS

Percentage Total wastage, %5

10.0±0.1

41.6±0.1

*

Wastage due to
non-infectious causes, kid/doe

0.21±0.18 (n= 14)

0.62±0.19 n=13)

NS

Percentage non-infectious
wastage, %

8.4±0.1 (n= 14)

37.2±0.1 n=13)

*

1Parturiation
was used as a sign of animal having conceived since neither
ultrasonic nor progesterone were used to verify pregnancy.

†Toxoplasma
gondii and S. bovis were isolated in this aborted material.

SL = Significance level;
NS = P>0.05; * = P<0.05

Of the two
goats whose kids died within 24 hours in C group, the diagnosis was postnatal
weakness leading to secondary septicaemia. However, for the three goats whose
kids died within 24 hours in the S group, the diagnosis for one of them was
purulent bronchopneumonia while the other two was inconclusive. One of the two
goats that aborted in the C group had twin fetuses from which Toxoplasma
gondii and Streptococcus bovis were isolated.

Prolificacy
for S animals was similar (P>0.05) to that of C animals. Total reproductive
wastage was not significantly (P>0.05) different between the two groups although
it was lower for S than C animals. However, percentage total reproductive
wastage was different (P<0.05; Table 2).

Birth weights
were similar (P>0.05) between S and C animals. Multiples weighed lower (P<0.001)
than singles. Multiples kids in both S and C animals weighed similar
(P>0.05). Kids born as singles had similar (P>0.05) weights at birth for S and
C. Does parturition weight had a significant effect (P<0.001) on kid birth
weights (Table 3).

Table 3.
Body weight and condition score of Tswana goats

Parameter

Supplemented

Control

SL

At mating

n=18

n=19

Body weight, kg

39.8±0.90

38.8±0.88

NS

Condition score1

2.81±0.17

2.74±0.17

NS

At two weeks prior to
parturition

n=15

n=14

Body weight, kg

43.9±1.3

39.1±1.4

*

Condition score

2.83±0.16

1.89±0.16

***

At parturition

n=14

n=14

Body weight, kg

40.1±1.3

35.1±1.3

*

1Condition
score: 1= thin, 5 = fat, according to Karua (1990)

SL = Significance level;
NS = P>0.05; * = P<0.05; *** = P<0.001

At mating, the
two groups had similar body weight (P> 0.05) and body condition score (P> 0.05)
for S and C animals (Table 3). However, two weeks prior to parturition S animals
exhibited higher body weight (P<0.05) and high BCS (P<0.001) than C animals. At
parturition S animals were still heavier (P<0.05) than C animals. Doe
parturition weights of S (r=0.617, P<0.001) and C (r=0.550, P<0.05) were
positively correlated to kid birth weight. However, when singles were removed
from the analysis, doe parturition weight of S animals was highly correlated
(r=0.756, P<0.001) to birth weight while correlation of doe parturition weight
of C to birth weight was not significant (r=0.250, P>0.05).

Total protein,
albumin, calcium, phosphorus, copper, zinc, urea, triglycerides and cortisol
were similar (P>0.05) between the two groups (Table 4).

Table 4.
Blood parameter of Tswana goats at two weeks prior to parturition

A significant
difference between S and C animals was observed on cholesterol, haematocrits, T3
(P<0.05) and T4 (P<0.01).

Discussion

In Botswana, goats kidding during the later part of the dry season (August to
September) would have been mated at the end of the wet season (April) when
nutrition would be adequate for ovarian activities and this period also
coincides with decrease in day length. Mating at this time means that the level
of sexual activity is high and may result in multiple births. However, the rest
of pregnancy goes through a period of shortage of nutrients especially at the
last trimester when the fetus growth rate is high. As a result malnutrition may
results in abortion in goats.

The insignificant and small difference between S and C animals in the proportion
of goats that either gave birth or aborted (pregnancy rate) in the present study
may be due to nutrition. Toxoplasma gondii has previously been associated
with goats with a history of abortion in Botswana (Binta et al 1996, Binta et al
1998a). However, it is suggested that in the present study, infectious agents
were not the prime cause of reproductive wastage. Previous data (Madibela et al
2002) with the same flock of animals showed that fertility and the proportion of
animals that gave birth during the wet season was similar between the
supplemented and control animals. If the ovarian activity of the animals in the
present study was the same; the reduced pregnancy rate in C group would then be
due to embryonic loss as the dry season progress.

The consistent twinning of 50% in Tswana goats (APRU 1987, APRU 1989, Madibela
et al 2002) may be indicative of a genetic attribute of this breed. Prolificacy
rate for S animals was close to 2 kids/doe and this may contribute substantially
to farmer’s productivity. This indicates that if abortion and neonatal death are
reduced, Tswana goats would have high productivity. When infectious causes were
removed from the analysis, C animals still had high reproductive wastage. Lower
body weight and BCS at two weeks prior to parturition and at parturition of C
animals showed that when pregnant goats are undernourished, reproductive wastage
would occur. Besides the problem of abortion due to undernutrition, neonates are
weak and are susceptible to infection. In the present study kids from multiple
births were weak at birth.

Lack of difference in kid birth weight indicate that the high dam liveweight and
BCS of S animals did not benefit kid birth weights, which was consistent with
findings of Madibela et al (2002). Doe parturition weight was positively
correlated to birth weight of multiple born kids in S but not in C group. This
is an unexpected finding since C animals were nutritionally stressed and they
were expected to produce kids of low birth weight. This may be due to enhanced
fetal growth as a result of stimulated placental growth and function when
females are subjected to nutrient restriction at mid pregnancy (Robinson 1990,
Wallace et al 1997, Perry et al 1999 and Robinson et al 1999).

Thyroid hormones concentrations are nutritionally sensitive (Rae et al 2002). In
the present study the difference in the concentrations of thyroid hormones
between the two groups may be associated with the difference in reproductive
wastage. Manalu et al (1997) did not found difference in T3 between
aborted goats and dams bearing single and twin kids. T3 was found to
be high in non-pregnant, indicating that the increase in T3 was not
related to pregnancy (Manalu and Sumaryadi 1999). However, the reproductive
physiology of non-pregnant animals and those that aborted is not the same,
hence; it would be invalid to compare the two. Rae et al (2002) found that
undernutrition in pregnant sheep results in low plasma T3. The
viability of neonatal kids contributed to reproductive wastage in the present
study and according to Robinson (1990) there is a positive correlation between
neonatal survival and plasma T3 and T4 concentrations. In
the present study thyroid hormones of kids were not measured. However, Rae et al
(2002) found that foetal T3 and T4 concentrations were low
in response to maternal undernutrition which may affect gonadaldevelopment of offsprings.

The results of cortisol concentrations cast doubts to its direct involvement in
reproductive wastage. Manalu et al (1997) found no difference in average serum
cortisol level of aborted, single and twin bearing does. In addition, Manalu and
Sumaryadi (1999) reported no relation between cortisol concentrations during
pregnancy with lamb birth weight. In the present study birth weights in the two
groups were similar thus maternal serum cortisol may not have contributed to
reproductive wastage or kid viability. Romero-R et al (1998) found that maternal
cortisol concentration for normal delivering goats to be 35.5nmol/l at
peripartum, which is 21.5 and 41.9% higher than cortisol levels of S and C
animals of the present study respectively. Those animals that aborted were found
to have even higher values of cortisol at the time of abortion leading the
authors to conclude that cortisol was associated with abortion.

Values of total protein in the present study were similar, but at the lower end
of the normal range for goats. Although it has low affinity for thyroid
hormones, albumin has high binding capacity due to its high concentration in
plasma (Cunningham 1997). In the present study, the difference in albumin,
albeit in small quantities, may have contributed to a significant difference in
thyroid hormones between the two groups. Blood minerals did not contribute
directly to differences in reproductive wastage. Gray et al (1990) reported
calcium levels of supplemented goats that were similar to the value of S animals
in the present study. Phosphorus was found to be higher while copper to be lower
than values obtained by Gray et al (1990). Urea levels were found to be similar
to values for goats in Botswana (Gray et al 1990). Protein content of pasture
for foraging goats during periods similar to those of animals in the present
study was reported by APRU (1983/4) to be 12g/kg. High protein in browse diet
may have resulted in high serum urea. In addition, BCS of C animals were lower
than those of S, indicating that animals’ nutrient requirements were partly met
through mobilization of body reserves. Pambu-Gollah et al (2000) found that dry
season kidding goats in South Africa were not able to maintain glucose
homeostasis during pregnancy but their plasma urea levels were elevated during
the last month of pregnancy.

In the present study, cholesterol level was higher in S group but it is not
clear how the trend would have progressed over time. This is because according
to Kaneko (1989), the net effect of thyroid hormones on cholesterol metabolism
is to increase the rate of its catabolism by the liver, thereby lowering
cholesterol. Even though triglyceride levels were similar between the two
groups, C animals were under metabolic stress, which was consistent with their
lower body condition at two weeks prior to parturition and at parturition.
Therefore, the lower levels of cholesterol and triglycerides in C animals are
consistent with the underlying negative energy balance of these animals.

Conclusions

Supplementary feeding of does during
pregnancy offset detrimental effects of maternal nutritional stress and hence
reducing reproductive wastage in goats.

Acknowledgements

The summary of this paper was presented
at an International Conference of the British Society of Animal Science,
University of York. England. [Madibela O Rand Segwagwe B E V (2003)
Nutritional effects on maternal blood metabolites and on outcome of pregnancy of
dry season kidding Tswana goats. Paper No 83]

The authors would like to thank National Veterinary Laboratory for their
technical input and A. Human (University of Pretoria, SA) for hormonal analysis.
Prof. J J Robinson (Scottish School of Agriculture, Aberdeen, Scotland) is
recognized for comments on the initial draft of this manuscript. This study was
funded by Botswana’s Ministry of Agriculture.

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